Bilirakis has worked in various capacities. He worked as a steelworker while in college in Pittsburgh and later worked as an engineer. Bilirakis spent the majority of his professional career as an attorney and also taught law classes. He served as a municipal judge in both Tarpon Springs and New Port Richey, Florida.

He made his first run for office in 1982, contesting the newly created and then politically balanced 9th District. He narrowly defeated State RepresentativeGeorge Sheldon by 4,300 votes. However, he was reelected with 78 percent of the vote in 1984 and was reelected 10 more times, never facing serious opposition. He even ran unopposed in 1988, 1994, 1998 and 2004.